Acanthopagrus oconnorae, a new species of seabream (Sparidae) from the Red Sea

Abstract A new species of sparid fish, Acanthopagrus oconnorae, is described based on 11 specimens collected in the shallow (0–1 m depth) mangrove‐adjacent sandflats of Thuwal, Saudi Arabia. The new species is distinguished from its congeners by the following combination of characters: second anal‐fin spine 12.8%–16.6% of standard length (SL); 3½ scale rows between the fifth dorsal‐fin spine and lateral line; suborbital width 5.7%–6.7% of SL; eyes positioned at the anterior edge of the head, often forming a weakly convex break in an otherwise gently curved head profile, when viewed laterally; caudal fin light yellow with black posterior margin (approximately half of fin); anal fin dusky grey, with posterior one‐fifth of the fin light yellow; black streaks on inter‐radial membranes of anal fin absent. The most similar species to A. oconnorae is Acanthopagrus vagus, which differs by the presence of a w‐shaped anterior edge of the scaled predorsal area, a more acute snout and black streaks on the inter‐radial membranes of the anal fin. Phylogenetic placement and species delimitation of A. oconnorae are discussed based on COI, CytB and 16S sequences. It is hypothesized that ecology and behaviour explain how this species avoided detection despite its likely occurrence in coastal areas of the Red Sea with historically high fishing pressure.

Recent field investigations on the Red Sea coast of Thuwal, Saudi Arabia, yielded several specimens of Acanthopagrus with yellowish-fin colouration. Nonetheless, after detailed morphological and genetic comparisons with other similar species, the authors conclude that these specimens represent a previously undescribed species. Here the authors describe Acanthopagrus oconnorae sp. nov.
based on 11 specimens collected from Thuwal, Saudi Arabia.

| Specimen collection and morphological data
The authors collected 11 specimens of A. oconnorae sp. nov in shallow water (maximum 1 m depth at high tide) immediately adjacent to the mangroves near Thuwal in the central Red Sea (22.308367 N,39.091016 E) ( Figure 4). The first three specimens were collected using conventional hook-and-line gear, and the remaining eight specimens were captured using a tidal trap (Figure 1). A fin clip of each specimen was preserved in 96% ethanol for further molecular analysis. All morphologically analysed specimens were photographed alive, anaesthetized with lethal doses of MS-222 (following Popovic et al., 2012) and then transported to the laboratory for further detailed photographs and analysis. All counts and measurements were made following Hubbs and Lagler (1964) with modifications from  using a digital calliper with an accuracy of 0.1 mm. The dorsal-most scales below the fifth and first dorsal-fin spines, respectively, were counted as a half scale. Counts and measurements were taken on the left side of the body wherever possible.
The calculated value for the second anal-fin spine length/third analfin spine length was abbreviated as 2AS/3AS. The authors then compared the meristics and morphometrics of their specimens to all nominal species of Acanthopagrus (Hasan et al., 2020;Iwatsuki, 2013).

| Material examined in addition to type specimens
For a comparative morphometric and phylogenetic investigation among Acanthopagrus species, specimens of several other Western Indian Ocean representatives of Acanthopagrus spp. and Rhabdosargus haffara and Sparidentex hasta were obtained (see Supporting Information Table S1). One specimen of A. berda and five specimens of R. haffara (Fabricius in Niebuhr, 1775) were captured using the same tidal trap mentioned earlier. Individuals of R. haffara were released after a photograph was taken and a fin clip was collected. Specimens of A. arabicus, A. bifasciatus, A. catenula and A. sheim were obtained from a fish market in Dammam, on the eastern coast of Saudi Arabia.
All specimens from the Damman fish market were caught by local fishermen in the Arabian Gulf except for A. catenula, which was shipped to the Dammam fish market from Oman.
Initial morphological identification of all specimens collected from Dammam was performed by Y.J.L. Whole specimens from the Dammam fish market were further analysed in the Reef Ecology Laboratory at the King Abdullah University of Science and Technology (KAUST) by V.N.P. and L.P.-A. The morphological identification of these species was further confirmed by barcoding of COI and 16S fragments against available sequences on GenBank, including the hologenetypes of A. sheim and A. arabicus (Iwatsuki, 2013

| Molecular data, phylogenetic analysis and DNA-based species delimitation
The authors used the Qiagen Blood and Tissue Kit with 56 C overnight incubation for all DNA extractions. The mitochondrial fragments of the regions COI, CytB and 16S were amplified. COI was amplified using the universal fish primers FishF1 and FishR2 (Ward et al., 2005), CytB using the primers Cyb9 (Song et al., 1998) and Cyb7 (Taberlet et al., 1992) and 16S using the primers 16SF and 16SR (Palumbi, 1996). The thermal profiles for COI, CytB and 16S were as follows: 15 min of denaturation at 95 C, followed by 35 cycles of 30 s of denaturation at 94 C, primer annealing for 1 min at 50 C and 1 min extension at 72 C, with a final extension of 10 min at 72 C.
Published partial sequences of COI, CytB and 16S of all available fishes of the genus Acanthopagrus were downloaded from GenBank (Sayers et al., 2011) to build a phylogeny and position A. oconnorae in a phylogenetic context. Details of the accession numbers of the sequences along with supporting data are provided in Supporting Information Table S1. All sequences were edited and concatenated into alignments using the alignment function based on the MAFFT algorithm (Kazutaka et al., 2009) in GENEIOUS 2021Kearse et al., 2012). Some of the species of this study are missing at least one of the fragments (COI, 16S or CytB) in public repositories. Phylogenetic analysis was performed with concatenated partial sequences of COI, CytB and 16S using maximum likelihood on the online platform for IQtree (Trifinopoulos et al., 2016). This approach allows us to include samples missing one locus, thus maximizing the number of samples and species in the phylogenetic analysis. The branch support was analysed with SH-aLRT (Anisimova et al., 2011), aBayes support (Guindon et al., 2010) and ultrafast bootstrap (Minh et al., 2013).
For DNA-based species delimitation, the authors used two methods based on distance matrices of the COI alignments and one method based on the COI phylogenetic tree. For the first two approaches, they used genetic distance matrices based on the COI alignments using the Kimura 2-parameter as inputs for the Assemble Species by Automatic Partition (ASAP, Puillandre et al., 2021)

| Ethics statement
The collection of live individuals in this study was carried out under the ethics protocol numbers 18IACUC14 and 19IACUC03 issued by the KAUST Institutional Animal Care and Use Committee. The exception is the first individual which was caught in the course of recreational fishing. All subsequent live individuals targeted for this study followed the ethics protocols described in Section 2.1.

| Nomenclatural acts
The species names presented in this article comply with the Interna-

| Distribution and habitat
Currently this species is known from the mangrove-adjacent sandflats and mangrove-encircled pools of Thuwal, Saudi Arabia, in the central Red Sea. All specimens were caught in very close proximity to the mangrove habitat. All the trapped specimens were captured on sandflat shelves with very shallow water (maximum 1 m depth at high tide) near coastal stands of mangroves (Avicennia marina). Individuals of A. oconnorae appear to commonly utilize a specific type of habitat, cooccurring with A. berda, R. haffara, Pomadasys argenteus, Gerres longirostris, Monodactylus argenteus, Albula glossodonta and Crenimugil crenilabis.

| Common name
The

| Comparisons
Selected characteristics highlighting the morphological taxonomy differences between A. oconnorae sp. nov. and other similar species in the Western Indian Ocean region are summarized in Table 2. The three species most similar to A. oconnorae are illustrated in Figure 3 along with their geographical distribution in Figure 4. Acanthopagrus species with similar colouration and Western Indian Ocean distribution are shown in Supporting Information Figure S2.

A. oconnorae shares somewhat similar fin colouration with
A. arabicus, A. sheim and A. vagus. All have more or less yellow or yellowish pelvic fin and anal fin. Of these, A. oconnorae is the most similar to A. vagus from the south-western Indian Ocean (Table 2) A. oconnorae differs from both A. arabicus and A. sheim in the count of scale rows between the fifth dorsal-fin spine base and lateral line (3½ vs. 4½) and in fin colouration (see Table 2). A. arabicus has bright yellow pelvic, anal and ventral edges of the caudal fin and no black streaks proximally on inter-radial membranes between yellow anal-fin rays, and A. sheim has pelvic fins usually whitish with pinkish tinge, anal fin mostly yellow with black markings in the middle, ventral edge of caudal fin usually orange pink or rarely yellowish, with black streaks present on inter-radial membranes of fin rays (Iwatsuki, 2013;Sergey Bogorodsky, pers. comm.). Nonetheless, two or three series of small black blotches are present on the proximal inter-radial membranes between the dorsal-fin rays in A. sheim, whereas A. oconnorae has small, irregular blotches infrequently (Supporting Information Figure S1).
A. oconnorae is presumably a Red Sea endemic. It is easily distinguishable from the two other currently recognized species of Acanthopagrus reported from the Red Sea (A. berda and A. bifasciatus). A. berda has the same number (3½) of scale rows between the fifth dorsal-fin spine base and lateral line as A. oconnorae, but it has a much deeper body, uniformly dark grey to brown body and median fins, and a distinctive concavity at the ventral edge of the first two infraorbitals (Iwatsuki & Heemstra, 2010). A. bifasciatus and A. catenula are quite dissimilar to A. oconnorae by their conspicuous black bars across the faces and black pelvic and anal fins and bright yellow dorsal, pectoral and caudal fins (Iwatsuki & Heemstra, 2011). Moreover, they have 5½-6½ and 4½ scale rows, respectively, between the fifth dorsal-fin spine base and lateral line (Iwatsuki & Heemstra, 2011), whereas A. oconnorae has 3½ scale rows.

| Phylogenetic analysis
Here the authors present the most comprehensive molecular phylogeny of the genus Acanthopagrus to date, including 17 of the 20 currently described species and the new species described here (A. oconnorae) (Figure 6; Appendix 1). The maximum likelihood tree supported by Bayesian posteriors of 1 indicates that all the specimens the authors collected of A. oconnorae form a monophyletic group and that its closest relative (Bayesian posterior support 0.98) is A. vagus, whose geographic distribution does not include the Red Sea (it is present in the Indian Ocean from South Africa to southern Mozambique, Figure 4) (Iwatsuki & Heemstra, 2010). With Bayesian posterior support of 1, the closest species to the clade composed of A. oconnorae and A. vagus is A. sheim, which is known only from Pakistan and the Arabian Gulf. These results were supported by the K2P distances of COI and 16S (Table 3). The COI matrix indicates that the closest species to A. oconnorae is A. vagus with a mean distance of 7.2% followed by A. sheim with a mean distance of 7.9% and A. arabicus with a mean distance of 9.4% (Table 2). As noted by previous authors (Carpenter & Johnson, 2002;Hasan et al., 2020)

| DISCUSSION
The Red Sea is a biodiversity hotspot (Dibattista et al., 2016a(Dibattista et al., , 2016b, with one of the highest levels of endemism in the world. With 14.6% of Red Sea fish species found nowhere else, the Red Sea is behind only the Hawaiian Islands (30.4%) and Easter Island (21.7%) in its proportion of endemism for fishes (Bogorodsky & Randall, 2018). Such a high biodiversity and endemism rate appear to be firmly linked with the unique environmental characteristics (e.g., high temperatures and salinity) found in the Red Sea . Due to its status as a relatively understudied locality , the potential for the discovery of new Red Sea species remains high. In some cases, careful examination of widespread taxa has revealed cryptic diversity (e.g., Coleman et al., 2016;Priest et al., 2016), indicating that the level of endemism in the Red Sea may be underestimated. As a relatively large (maximum 27 cm total length) sparid fish inhabiting shallow coastal waters in close proximity to a large human population, the newly described A. oconnorae exemplifies this potential.
Endemic lineages in the Red Sea are, in most cases, derived from their Indian Ocean counterparts (DiBattista et al., 2013(DiBattista et al., , 2015, potentially resulting from allopatric divergence during Pleistocene isolation (Klausewitz, 1989 fauna more than 200 years ago, frequently using material from local fishermen (see Berumen et al., 2019). Modern local fishing operations still focus on reef fish, employing hand-lines, nets, traps and other methods (Jin et al., 2012;Tesfamichael & Pauly, 2016), and these are mostly utilized in the slightly deeper waters of the fringing reefs or further away from the coastline. Therefore, very little fishing effort is concentrated in the very shallow waters immediately adjacent to or encircled by mangrove habitats.
A potential hypothesis to explain the prior lack of detection of A. oconnorae is that the species' behaviour is to remain in very close proximity to the mangroves, whereas species such as A. berda venture out into the deeper waters of the fringing reef (Garratt, 1993), where they are routinely captured in the local fisheries (notably, the holotype of A. berda was collected by Forsskål between 1761 and 1763 during the Danish Arabian expedition). Further work on the fine-scale distribution, habitat use and movement ecology of A. oconnorae could test this hypothesis.
The discovery of a relatively large species in such proximity to inhabited areas further underscores the need for immediate conservation actions. Several large coastal developments are underway in Saudi Arabia; care must be taken to avoid the degradation of habitats such as the mangrove and sandflats that A. oconnorae appears to utilize.
Such habitat specialization is likely to occur with numerous lessconspicuous species (e.g., Atta et al., 2019;Troyer et al., 2018); there are potentially many additional undescribed species in the Red Sea remaining to be discovered in families such as the Gobiidae (e.g., Coker et al., 2018).